Organic Diets Significantly Lower Children s Dietary Exposure to Organophosphorus Pesticides
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1 ehponline.org Organic Diets Significantly Lower Children s Dietary Exposure to Organophosphorus Pesticides Chensheng Lu, Kathryn Toepel, Rene Irish, Richard A. Fenske, Dana B. Barr, and Roberto Bravo doi: /ehp.8418 (available at Online 1 September 2005 The National Institute of Environmental Health Sciences National Institutes of Health U.S. Department of Health and Human Services
2 Organic Diets Significantly Lower Children s Dietary Exposure to Organophosphorus Pesticides Chensheng Lu 1, Kathryn Toepel 2, Rene Irish 2, Richard A. Fenske 2, Dana B. Barr 3, Roberto Bravo 3 1 Department of Environmental and Occupational Health, Rollins School of Public Health, Emory University, Atlanta, GA, USA. 2 Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, USA. 3 National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA, USA. Corresponding author Chensheng Lu 1518 Clifton Road, NE, Room 226 Atlanta, GA (404) , (404) (fax) clu2@sph.emory.edu 1
3 Running title: Children s dietary pesticide exposure. Article descriptor: Children s health. Key words: children s pesticide exposure, dietary pesticide exposure, organic diet, organophosphorus pesticides, urinary biomonitoring, chlorpyrifos, malathion. Abbreviations: CMHC, 3-chloro-4-methyl-7-hydroxycoumarin DEAMPY, 2-diethylamino-6-methylpyrimidin-4-ol DVWA concentration, daily volume-weighted average concentration IMPY, 2-isopropyl-6-methyl-pyrimidin-4-ol LOD, limits of detection MDA, 2-[(dimethoxyphosphorothioyl)sulfanyl]succinic acid OP, organophosphorus PDP, Pesticide Data Program TCPY, 3, 5, 6-trichloro-2-pyridinol USDA, United State Department of Agriculture USEPA, United State Environmental Protection Agency Acknowledgments This study was supported by the U.S. Environmental Protection Agency (EPA), Science to Achieve Results (STAR) program (RD ). Its contents are solely the responsibility of the authors and do not necessarily represent the official view of the U.S. EPA. We would like to express our sincere appreciation to the children who participated and to their parents who greatly assisted in this study. We also thank Mr. Patrick Sande s assistance in collecting daily specimen samples, Amanda Bishop, Paula Restrepo, Robert Walker, Johnny Nguyen, and Donna Walden at CDC for their help with sample analysis, and the Mercer Island School District in Mercer Island, WA for granting our request of circulating the study flyers in their elementary schools for subject recruitment. The authors declare they have no competing financial interests. 2
4 Outline of section headers Abstract 4 Introduction 5 Methods 6 Results 8 Discussion 10 Conclusion 14 References 15 Tables 18 Figure Legends 20 Figures 21 3
5 Abstract We utilized a novel study design to measure dietary organophosphorus pesticide exposure in a group of elementary school-age children through urinary biomonitoring. We substituted most of children s conventional diets with organic food items for 5 consecutive days, and collected two, first morning and before the bedtime voids, daily spot urine samples throughout the 15-day study period. We found that the median urinary concentrations of the specific metabolites for malathion and chlorpyrifos decreased to the non-detect levels immediately after the introduction of organic diets and remained non-detectable until the conventional diets were re-introduced. The median concentrations for other organophosphorus pesticide metabolites were also lower in the organic diet consumption days, however, the detection of those metabolites were not frequent enough to show any statistical significance. In conclusion, we were able to demonstrate that an organic diet provides a dramatic and immediate protective effect against exposures to organophosphorus pesticides that are commonly used in agricultural production. We also concluded that these children were most likely exposed to these organophosphorus pesticides exclusively through their diet. To our knowledge this is the first study to employ a longitudinal design with a dietary intervention to assess children s exposure to pesticides. It provides new and persuasive evidence of the effectiveness of this intervention. 4
6 Introduction The National Research Council s 1993 report entitled Pesticides in the Diets of Infants and Children concluded that dietary intake represents the major source of pesticide exposure for infants and children, and this exposure may account for the increased pesticide-related health risks in children compared to adults (NRC 1993). However, direct quantitative assessment of dietary pesticide exposure in children to support this conclusion is no simple task: several studies (Adgate et al. 2000; Fenske et al. 2002; Gordon et al. 1999; MacIntosh et al. 2001) have analyzed pesticides in representative samples of children s food, and only two have utilized biological monitoring to specifically examine dietary exposures (Curl et al. 2003; MacIntosh et al. 2001). The paucity of exposure data renders the debate over pesticide-related health risks in children controversial (Flower et al. 2004; Garry 2004; Reynold et al. 2005). Nevertheless, those studies have provided valuable information in regard of the evidence of dietary pesticide exposure among children, and have prompted the needs to improve research methods in order to better assess children s exposure to pesticides through dietary intake. The primary objective of this study is to utilize a novel study design to determine the contribution of daily dietary pesticide intake to the overall pesticide exposure in a group of elementary school-aged children using a longitudinal approach. We only report results of urinary specific metabolites of organophosphorus (OP) pesticides, a group of insecticides known to cause neurological effects in animals and humans, for the summer 2003 sampling period here. Results of pyrethroid pesticides for the same summer 5
7 sampling period, as well as results from other sampling periods will be reported as soon as it becomes available. Methods Subject recruitment Twenty-three children ages 3-11 years were recruited from local public elementary and Montessori schools in suburban Seattle, WA area. A letter and a fact sheet describing the study were sent home with children. Families that were interested in participating contacted the research group directly by phone or . Schools did not provide any assistance in recruiting subjects. A screening questionnaire was conducted over the phone to confirm the eligibility, which includes children exclusively consuming conventional diets, spending most of their time in one residency, and the willingness from parents or caregivers to provide assistance in collecting specimen samples and other study related information. Once a subject was enrolled, an in-house appointment was made to go over the study protocol and to obtain written consent from parents and older children, or oral assent from younger children. A questionnaire was also administered during this appointment that asked about household pesticide use to account for other sources of possible pesticide exposure. The University of Washington Human Subject Division (# ) approved the use of human subjects in this study. Sampling period Each child committed to a 15-consecutive-day sampling period, which consisted of 3 phases. Children consumed their conventional diets during phase 1 (day 1 to 3) and phase 3 (day 9 to 15). During phase 2 (day 4 to 8), organic food items were substituted for most of children s conventional diet, including fresh fruits and vegetables, juices, 6
8 processed fruit or vegetables (e.g. salsa), and wheat- or corn-based items (e.g. pasta, cereal, popcorn or chips) for 5 days. These food items are routinely reported to contain OP pesticides (USDA 2003). OP pesticides are not regularly detected in meats and dairy products, and therefore these food items were not substituted. All organic food items were purchased by the research staff from a single grocery store. Parents were asked to request organic foods for their children in phase 2 with the goal of exactly replacing the items the children would have normally eaten as part of their conventional diet. This method ensured that any detectable change in dietary pesticide exposure would be attributable to the organic food rather than a change in the diet. Each child s daily dietary consumption was recorded by a parent in a food diary throughout the study period. Organic food items, mostly fresh vegetable and fruit and juices, were purchased prior to and during the study period and analyzed by one of the United States Department of Agriculture (USDA) Pesticide Data Program (PDP) contracted laboratories in Yakima, WA to confirm that the food items were indeed free of pesticides. No OP or other pesticides were detected in any of the organic food items analyzed. Urine sample collection and analysis For 15 consecutive days, parents collected urine samples from their child s first morning and the last voids before bedtime. Urine samples were collected daily, refrigerated or maintained on ice prior to processing in the lab, and then stored at -20 C until pesticide metabolite analysis was performed (Olsson et al. 2004) at the National Center for Environmental Health in the Centers for Disease Control and Prevention in Atlanta, GA. Metabolites for selected OP pesticides, pyrethroid insecticides, and 7
9 herbicides in the urine samples were analyzed, and the limits of detection (LOD) for the OP metabolites are listed in Table 1. Data management Concentrations of OP specific metabolites were reported as three categories, detectable (> LOD), detectable but not quantifiable (< LOD), and non-detect (ND). For data analysis purpose, reported concentrations for samples with >LOD and <LOD were used, whereas 0 was assigned for non-detect samples. The daily volume-weighted average (DVWA) of OP pesticide metabolites was calculated (Equation 1) by averaging the metabolite concentration in the morning sample with the previous day s bedtime sample and then normalizing for the total volume of these two urine samples. In cases where only one of the two urine samples was collected, the metabolite concentration of the collected sample was used as the DVWA concentration. Urinary concentrations of OP metabolites were not adjusted by the creatinine or the specific gravity. DVWA (µg/l) = [C i (µg/l) x V i (ml)] / [V i (ml)] (1) where: C i, individual urinary concentration, V i, volume of the correspondent spot urine sample. Results Frequencies of detection (Table 1) for 5 OP metabolites in 724 urine samples collected from children throughout the study period differed during the conventional diet phases (phase 1 and 3), and varied significantly between conventional and organic diet phases for two metabolites (MDA, metabolite of malathion; TCPY, metabolite of chlorpyrifos). These differences probably reflect the frequency of the uses of these OPs in agricultural production, in which malathion and chlorpyrifos are all commonly used on 8
10 fruits, vegetables, or wheat. Para-nitrophenol concentration was quantified but not included in this report because it is no longer considered a specific biomarker for methyl parathion exposure (Barr et al. 2002). The distributions of DVWA concentrations for MDA and TCPY during the 3 study phases (Figures 1 and 2) highlight the effect of organic food consumption on OP pesticide exposures in children. All children s urine samples contained MDA and TCPY when they enrolled in this study. Immediately after the introduction of organic food to children s diets, median urinary MDA and TCPY concentrations decreased to the ND level and remained non-detectable until conventional diets were re-introduced after 5 days of organic food consumption. The DVWAs for MDA and TCPY in the organic diet phase were significantly lower than the levels in either conventional diet phases (one-way ANOVA, p<0.01, Table 1). The substitution of organic diets has no effect on the dietary exposures for diazinon (parent OP pesticide for IMPY), methyl pirimiphos (parent OP pesticide for DEAMPY), and coumaphos (parent OP pesticide for CMHC). These OP pesticides are either less commonly used in agriculture or has restricted use, such as coumaphos, which is registered for use in livestock only. Discussion Concerns were raised by the National Research Council s 1993 report, Pesticides in the Diets of Infants and Children regarding the quantitative and qualitative differences in the toxicity of, and the exposure to pesticides in children, as compared with adults. This report recognized that dietary intake of pesticides represents the major source of exposure for infant and children, and concluded that the differences in dietary exposure to pesticide residues account for most of the differences in pesticide-related health risks that 9
11 were found to exist between children and adults. Dietary pesticide exposure was commonly assessed by collecting duplicate food samples from the study subjects. This method assumes that the pesticide residues measured in the food samples represent the best surrogate measurements for the dietary intake of pesticide residues, however, the correspondence of pesticide residues in the duplicate food samples and the absorbed pesticide dose measured in biological samples has rarely been determined. The objective of this study was to assess dietary pesticide exposures in individual children by substituting their conventional diets with organic food items. The results from this study should provide the most direct and relevant data for assessing children pesticide exposure through dietary intake. An important aspect of this study was to assure that the study protocol did not alter children s diets, qualitatively speaking, from their normal consumption patterns. Children may reject organic food items because of the taste or appearance, and therefore restricted themselves to a rather simple and less diverse diet during the organic diet phase. Consequently, this may confound the results whether potentially observed differences in dietary pesticide exposures truly result from consuming organic food items, not because of the changes in children s diets. A few trial runs with different children in the same age range were performed prior to the study in order to evaluate children s acceptance of organic versions of the food items they regularly ate. Parents commented about their child s response and found that most items were acceptable by their children especially with children whose parents considered not very selective in foods. It was then determined that it would be vital to recruit children who are adventurous with food taste and appearance. According to the food diaries, children consumed approximately 2 10
12 more items of fresh produce (including juices) and wheat/rice/soybean based food items in the organic diet phase, comparing to the conventional diet phase. This finding indicates that the study protocol did not change children s regular diet consumption pattern, and therefore, should not bias the study results. We conclude that organic diets provide a protective mechanism against OP pesticide exposure in young children whose diets regularly consist of fresh fruit and vegetable, fruit juices, and wheat-containing items. Such protection is dramatic and immediate. This is particularly true for certain OP pesticides, such as chlorpyrifos and malathion as measured in this study, and is probably true for other OPs like azinphosmethyl, dimethoate, and acephate, which are only registered in agricultural production. These results are consistent with our previous finding (Lu et al. 2001) in which none of the dialkylphosphate compounds, a group of non-specific urinary OP pesticide metabolites, were found in one child from a pool of 110 children. The parents of this child reportedly provided exclusively organic produce and did not use any pesticides at home. Although we did not collect health outcome data in this study, it is intuitive to assume that children whose diets consist of organic food items would have a lower probability of neurological health risks, a common toxicological mechanism of the OP pesticide class. The persistent existence of OP pesticide metabolites in urine during the conventional diet periods raises a concern of the possible chronic exposures to OP pesticides in children. However, caution should be exercised when inferring exposures and health risks solely based on OP urinary metabolite levels. Several recent studies (Lu et al. 2005) have suggested that the OP metabolites can occur as degradates in food commodities, or in the environment (Morgan et al. 2004), although the amount of 11
13 metabolites measured only represents a fraction of OP pesticides. The presence of OP pesticide metabolites in foods and in the environment definitely complicates the estimation of absorbed pesticide doses, but should not be used to defend the less likelihood of direct dietary exposure to OP pesticides. If these degradates are absorbed efficiently and excreted unchanged in urine, they could contribute to the total OP metabolite levels. Future researches should be conducted to determine the magnitude of OP pesticide degradation in the environment and in foods, and the pharmacokinetics of those metabolites in humans. The lack of residential pesticide use as reported by the parents suggests that children in this study were exposed to OP pesticides exclusively from dietary intakes. Recent regulatory changes (USEPA 1998) aiming to reduce exposures in children have banned or restricted the use of many OP pesticides in the residential environment. This policy change no doubt greatly minimizes the OP pesticide exposures from residential use (Hore et al. 2005, Whyatt et al. 2004), however fewer restrictions have been imposed in agriculture. Chlorpyrifos and malathion residues in selected food commodities were regularly detected in selected food commodities (Table 2) as surveyed by annual USDA PDP from 2000 to These food items were also commonly consumed by the children in this study. Unfortunately, the trend in agricultural use of these OP pesticides was not assessable after 2002 because completely different commodities were monitored in The trade off of the heath risks caused by OP pesticide in children by such regulatory change, therefore, is difficult to quantify. Lastly, the magnitude of variability associated with urinary OP pesticide metabolite levels measured in this study is rather large; suggesting the scenario of dietary 12
14 exposure is sporadic with significant temporal variations. Such variability reflects the combination of the variation of OP pesticide residues found in food items, the probability of consuming those food items, and the relatively short biological half-lives of the OP pesticides in humans. The pitfall of such large variability is that it may compromise the true association between exposure and the outcome of interest. Despite this inherent variability, statistically significant trends were evident in this study. A study design incorporates with daily repeatable specimen collection over a period of time under the consideration of the pharmacokinetics of the non-persistent pesticides, like OPs, is preferable. Spot first morning void urine sample has been suggested as the best representative measurement for the daily OP pesticide exposure (Kissel et al. 2005). However, such approach is deemed not sufficient for assessing dietary exposure to OPs, or other exposure scenario in which subjects activities, such as dietary consumption pattern, are dynamic in nature. Many first morning void urine samples collected in this study have no detectable OP metabolite levels, whereas as the before bedtime urine samples collected in the previous day contained detectable metabolite levels. The opposite results were also observed in this study. Depending upon the timing of pesticide residue intake with certain meals, first morning void urine sample may not represent the true exposure. Considering the burden of study subjects and the cost of sample analysis, collecting before bedtime and fist morning void samples for assessing dietary exposure to OP pesticides seems to be the best choice. Children and their families participating in this study do not mirror the general population in U.S., and therefore attempt should not be made to infer this conclusion to other children. It will be of interest, from the regulatory and public health points of view, 13
15 to conduct additional studies that include children living in homes where residential pesticide use is common. If not applied according to label instructions, pesticide use in or around households may contribute more exposure to residents, particularly children, than dietary intakes (Lu et al. 2001). Conclusion In conclusion, we utilized a novel study design to provide a convincing demonstration of the ability of organic diets to reduce children s OP pesticide exposure and the health risks as may be associated with these exposures. Such reduction in exposure is dramatic and immediate, and is most obvious for OP pesticides, such as malathion and chlorpyrifos, that are commonly and predominately used in agricultural production, and have no or minimal residential uses. The findings for the OP pesticide exposure in children from this study, therefore, supports the conclusion made by the National Research Council s 1993 report that dietary intake of pesticides could represent the major source of exposure in infant and young children. 14
16 References Adgate JL, Clayton CA, Quackenboss JJ, Thomas KW, Whitmore RW, Pellizzari ED, et al Measurement of multi-pollutant and multi-pathway exposures in a probabilitybased sample of children: practical strategies for effective field studies. J Expo Anal Environ Epidemiol 10: Barr DB, Brave R, Weerasekera G, Caltabiano LM, Whitehead RD Jr., Olsson AO, et al Concentrations of dialkyl phosphate metabolites of organophosphorus pesticides in the US population. Environ Health Perspect 112: Barr DB, Turner WE, DiPietro E, McClure PC, Baker SE, Barr JR, et al Measurement of p-nitrophenol in the urine of residents whose homes were contaminated with methyl parathion. Environ Health Perspect 110: Curl CL, Fenske RA, Elgethun K Organophosphorus pesticide exposure of urban and suburban pre-school children with organic and conventional diets. Environ Health Perspect 111: Fenske RA, Kedan G, Lu C, Fisker-Andersen JA, Curl CL Assessment of organophosphorus pesticide exposures in the diets of preschool children in Washington State. J Expo Anal Environ Epidemiol 12: Flower KB, Hoppin JA, Lynch CF, Blair A, Knott C, Shore DL, et al Cancer risk and parental pesticide application in children of Agricultural Health Study participants. Environ Health Perspect 112: Food Quality Protection Act of Public Law, Garry VF Pesticides and children. Toxicol Appl Pharmacol 198: Gordon SM, Callahan PJ, Nishioka MG, Brinkman MC, O Rourke MK, Lebowitz MD, et al Residential environmental measurements in the national human exposure 15
17 assessment survey (NHEXAS) pilot study in Arizona: preliminary results for pesticides and VOCs. J Expo Anal Environ Epidemiol 9: Hore P, Robson M, Freeman N, Zhang J, Wartenberg D, Ozkaynak H, et al Chlorpyrifos accumulation patterns for child-accessible surfaces and objects and urinary metabolite excretion by children for 2 weeks after crack-and-crevice application. Environ Health Perspect 113: Kissel, J, Curl C, Kedan G, Lu C, Griffith W, Barr D, et al Comparison of organophosphorus pesticide metabolite levels in single and multiple daily urine samples. J Exp Anal Environ Epidemiol 15: Lu C, Fisker-Anderson J, Knutson D, Moate T, Fenske R Biological monitoring survey of organophosphorus pesticide exposure among pre-school children in the Seattle metropolitan area. Environ Health Perspect 109: Lu C, Bravo R, Caltabiano LM, Irish RM, Weerasekera G, Barr DB The presence of dialkylphosphates in fresh fruit juices: implication for organophosphorus pesticide exposure and risk assessments. J Toxicol Environ Health, 68: MacIntosh DL, Kabiru C, Echols SL, Ryan PB Dietary exposure to chlorpyrifos and levels of 3,5,6-trichloro-2-pyridinol in urine. J Expo Anal Environ Epidemiol. 11: Morgan MK, Sheldon LS, Croghan CW, Jones PA, Robertson GL, Chuang JC, et al Exposures of preschool children to chlorpyrifos and its degradation product 3,5,6-trichloro-2-pyridinol in their everyday environments. J Expo Anal Environ Epidemiol Sep 15; [Epub ahead of print]. 16
18 Olsson, A, Baker SE, Nguyen JV, Romanoff LC, Udunka SO, Walker RD, et al A liquid chromatography/ tandem mass spectrometry multiresidue method for quantification of specific metabolites of organophosphorus pesticides, synthetic pyrethroids, selected herbicides and deet in human urine. Anal Chem 76: National Research Council, Pesticides in the Diets of Infants and Children. Washington D.C. :National Academy Press. Reynolds P, Von Behren J, Gunier RB, Goldberg DE, Harnly M, Hertz A Agricultural pesticide use and childhood cancer in California. Epidemiology, 16: United State Department of Agriculture, Pesticide Data Program , [accessed 15 May, 2005]. United State Environmental Protection Agency, Children s Vulnerability to Toxic Substances in the Environment. EPA600/F/98/013: Washington DC: U.S. Environmental Protection Agency. Whyatt RM, Rauh V, Barr DB, Camann DE, Andrews HF, Garfinkel R, et al Prenatal insectivide exposures and birth weight and length among an urban minority cohort. Environ Health Perspect 112:
19 Table 1. Descriptive statistics for the daily volume-weight average (DVWA) concentrations of urinary metabolites for selected OP pesticides in the three study phases. Study Frequency Median Mean St. Dev. a Max. Phase N of Detection (µg/l) (µg/l) (µg/l) MDA b (LOD c = 0.3 µg/l) % d % d % d TCPY e (LOD = 0.2 µg/l) % f % f % f IMPY g (LOD = 0.7 µg/l) % 0 <LOD % 0 <LOD % 0 <LOD DEAMPY h (LOD = 0.2 µg/l) % % 0 <LOD % 0 <LOD CMHC i (LOD = 0.2 µg/l) % 0 <LOD % 0 <LOD % 0 <LOD a. St. Dev.; standard deviation. b. 2-[(dimethoxyphosphorothioyl)sulfanyl]succinic acid, metabolite for malathion. c. LOD; limit of detection. d. Significantly different (one-way ANOVA, p<0.01; Tukey test, phase 2 level significantly lower than levels in phase 1 and 3). e. 3, 5, 6-trichloro-2-pyridinol, metabolite for chlorpyrifos. f. Significantly different (one-way ANOVA, p<0.001; Tukey test, phase 2 level significantly lower than levels in phase 1 and 3). g. 2-isopropyl-6-methyl-pyrimidin-4-ol, metabolite for diazinon. h. 2-diethylamino-6-methylpyrimidin-4-ol, metabolite for methyl pirimiphos. i. 3-chloro-4-methyl-7-hydroxycoumarin, metabolite for coumaphos. 18
20 Table 2. Frequency of detection (%) a of chlorpyrifos and malathion residues in food items, and the frequency of consumption of those food items by children in summer Food item Chlorpyrifos Malathion Frequency of detection (%) detection (%) consumption by children b Apples Broccoli <1 5 Cantaloupe < Carrot < Celery Cherry Grape (and juice) 9 6 < Nectarine 6 2 < Orange Peach < 1 < 1 6 Rice < 1 < 1 < Strawberry (fresh) < Sweet Bell Pepper Tomato (canned) c Wheat/barley/soybean d a. Data from 2000 to 2003 USDA PDP reports. Blank cells represent items that were not analyzed for chlorpyrifos or malathion by PDP. b. Total consumption (servings) for children in 15 consecutive days. c. Consumed along with other food, such as pizza, pasta, and spaghetti. d. Including pizza, bagel, bread, cereal, cookies, chips, crackers, and noodles. 19
21 Figure Legends Figure 1. Box plots of daily volume-weighted average of malathion dicarboxylic acid (MDA) concentrations in children ages 3-11 for 15 consecutive days in which conventional and organic diets were consumed. Figure 2. Box plots of daily volume-weighted average of 3,5,6-trichloro-2-pyridinol (TCPY) concentrations in children ages 3-11 for 15 consecutive days in which conventional and organic diets were consumed. 20
22 20 MDA daily concentration (!g/l) Conventional Diets Organic Diets Conventional Diets -5 N = Sequential day Figure 1. 21
23 25 TCPY daily concentration (!g/l) N = 20 1 Conventional Diets Organic Diets Conventional Diets Sequential day Figure 2. 22
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